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ReviewCite this article: Colautti RI, Alexander JM,Dlugosch KM, Keller SR, Sultan SE. 2017Invasions and extinctions through the lookingglass of evolutionary ecology. Phil.Trans. R. Soc. B 372: 20160031.http://dx.doi.org/10.1098/rstb.2016.0031

Accepted: 30 August 2016

One contribution of 18 to a theme issue‘Human influences on evolution, and theecological and societal consequences’.

Subject Areas:ecology, evolution

Keywords:endangered species, niche theory, range limits,evolutionary genetics, plasticity, epigenetics

Author for correspondence:Robert I. Colauttie-mail: robert.colautti@queensu.ca

†Present address: Department of Ecology andEvolution, University of Lausanne, 1015 Lausanne,Switzerland.

Invasions and extinctions through thelooking glass of evolutionary ecologyRobert I. Colautti1, Jake M. Alexander2,†, Katrina M. Dlugosch3,Stephen R. Keller4 and Sonia E. Sultan5

1Department of Biology, Queen’s University, 116 Barrie Street, Kingston, Ontario, Canada K7L 3N62Institute of Integrative Biology, Department of Environmental Systems Science, ETH Zurich, Universitatsstrasse16, 8092 Zurich, Switzerland3Department of Ecology and Evolutionary Biology, University of Arizona, PO Box 210088, Tucson, AZ 85721, USA4Department of Plant Biology, University of Vermont, 111 Jeffords Hall, Burlington, VT 05405, USA5Department of Biology, Wesleyan University, 237 Church Street, Middletown, CT 06459, USA

RIC, 0000-0003-4213-0711; JMA, 0000-0003-2226-7913; KMD, 0000-0002-7302-6637;SRK, 0000-0001-8887-9213; SES, 0000-0001-8815-6437

Invasive and endangered species reflect opposite ends of a spectrum of eco-logical success, yet they experience many similar eco-evolutionarychallenges including demographic bottlenecks, hybridization and novelenvironments. Despite these similarities, important differences exist. Demo-graphic bottlenecks are more transient in invasive species, which (i)maintains ecologically relevant genetic variation, (ii) reduces mutationload, and (iii) increases the efficiency of natural selection relative to geneticdrift. Endangered species are less likely to benefit from admixture, whichoffsets mutation load but also reduces fitness when populations are locallyadapted. Invading species generally experience more benign environmentswith fewer natural enemies, which increases fitness directly and alsoindirectly by masking inbreeding depression. Adaptive phenotypic plas-ticity can maintain fitness in novel environments but is more likelyto evolve in invasive species encountering variable habitats and to be com-promised by demographic factors in endangered species. Placed in aneco-evolutionary context, these differences affect the breadth of the ecologi-cal niche, which arises as an emergent property of antagonistic selection andgenetic constraints. Comparative studies of invasions and extinctions thatapply an eco-evolutionary perspective could provide new insights into theenvironmental and genetic basis of ecological success in novel environmentsand improve efforts to preserve global biodiversity.

This article is part of the themed issue ‘Human influences on evolution,and the ecological and societal consequences’.

1. IntroductionGlobal biodiversity is increasingly under threat from human activity, which haselevated rates of extinction and invasion by several orders of magnitude abovehistorical averages [1,2]. The net result of increasing extinctions and invasions isa homogenization of global biodiversity that may be mitigated by two distinctbut complementary goals: (i) suppress long-term viability of invasive popu-lations and (ii) increase population growth rates of endangered nativespecies. Although eradication and enhancement are opposite conservationgoals, invasions and extinctions represent two extreme outcomes along asingle gradient of ecological success and therefore may be determined by thesame core set of ecological and genetic factors. In other words, invasions andextinctions of closely related species may be like reflections in Lewis Carroll’slooking glass [3], with similar elements reflecting opposite realities.

Several key environmental and demographic elements that affect populationgrowth and long-term persistence do not differ fundamentally between endan-gered and invasive species. Both experience strong demographic bottlenecks,

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hybridization with divergent lineages, and the demands ofsurviving and reproducing in novel and changing environ-ments. Yet, these common elements can lead to drasticallydifferent ‘realities’ or ecological outcomes, with invasivespecies expanding rapidly and endangered species spirallingtowards extinction.

One hypothesis for these contrasting fates is that endan-gered and invasive species possess distinct sets ofdevelopmental and life-history characteristics that are eitherbeneficial or detrimental in human-altered environments. Forexample, some species may be good invaders, because theyhave co-evolved with increasing human disturbances [4] orfluctuating environments [5] in their native ranges. However,a meta-analysis of 1813 species did not find evidence that inva-sive and threatened species possess contrasting traits [6]. It islikely that different characteristics are favoured at particularstages of invasion (i.e. transport, introduction, establishmentand spread) [7–9]. But many invasive species are close rela-tives of taxa that are not invasive [10,11], suggesting that anyfunctional basis for being invasive versus of conservationconcern is not often phylogenetically conserved. If develop-ment, life history or other phylogenetically conserved traitsdo not differ consistently between endangered and invasivespecies, then perhaps more transient ecological and geneticfactors are responsible for the varied ecological success ofspecies in nature.

How is it that even related species, having similar growthand life-history traits and encountering similar environmentaland demographic challenges, can end up at opposite ends onthe spectrum of ecological success? Here, we apply an eco-evolutionary perspective to explore some of the similaritiesand outline important but often overlooked differencesbetween invasions and extinctions. We focus on three areasof eco-evolutionary theory that reveal important differencesbetween endangered and invasive species likely to affect eco-logical success: the composition of ecologically relevantgenetic variation in natural populations, the genetic basisand evolution of phenotypic plasticity, and evolutionary con-straints on the ecological niche. Our overall goal is to examineinvasions and extinctions through the same lens of eco-evolutionary theory to suggest common principles for a unifiedapproach to both basic and applied research in these areas.

2. Genetic variationHuman activity exposes invasive and endangered species tonew adaptive landscapes in which natural selection is funda-mentally different from the ancestral environment [12].Comparing the evolutionary genetics of invasions and extinc-tions can shed new light on the fate of natural populationsexposed to novel and changing environments (figure 1).In this section, we compare the effects of demographic bottle-necks, inbreeding and admixture on invasive and endangeredspecies. We identify key differences that probably contributeto the very different population dynamics of invasionsand extinctions.

(a) Genetic variation and response to selectionEmpirical studies show that moderate to severe populationbottlenecks can be relatively common for both endangeredand invasive species [13–15]. However, post-bottleneckpopulation dynamics differ in several important ways that

translate to large differences in genetic diversity maintainedwithin populations (figure 1). One key difference is thelength of the bottleneck period [16], as this directly affectsthe rate at which genetic diversity is lost [17]. While paireddemographic and genetic data are rare for early stage inva-sions, the magnitude of genetic bottlenecks estimated fromneutral markers shows that, on average, invasive populationssuffer a detectable but relatively minor loss of genetic diver-sity [13]. This result suggests that most introduced populationsremain small for only a relatively short period before increas-ing again, because most introductions begin with a strongdemographic bottleneck involving a small fraction (! 1%) ofall individuals present in the native range. Endangered speciesfar more commonly experience extended periods of smallpopulation size, greatly increasing the loss of genetic diversity.Even if endangered populations do recover in census size, thegenetic effective size of the population (Ne) will recover slowlyas new mutations introduce variability back to the population.

Another factor mitigating loss of genetic diversity fromdemographic bottlenecks in invasive species is the high rateof gene flow common among introduced populations,which can promote ‘genetic rescue’ (alleviating inbreedingdepression; [18]) of inbred populations and ‘evolutionaryrescue’ (introduction of an adaptive variant; [19]) of mala-dapted populations [20–22]. Such increased gene flow isparticularly important within a metapopulation context,because the negative demographic and genetic consequencesof small population size and local extinction can be mitigatedby connectivity with other populations in the region[15,23,24]. Under this model, gene flow shares diversityamong populations so the metapopulation as a whole main-tains higher Ne and sustains the invasion even if individualinvasive populations are small. By contrast, declining popu-lations of endangered species tend to be few in number andhighly isolated, with little connectivity and opportunity forgenetic or evolutionary rescue. Efforts to increase populationconnectivity for endangered species may be particularly

extinction

ecological constraint

sustained transient

spreading

expansion

evolutionary andgenetic rescue

declining

contraction

time

nichealtered

hybridization

demographicbottlenecks

altered VGand G×E

novelenvironments

outbreedingdepression

stochastic forces andgenetic constraints

limit adaptive evolution

invasion

ecological release

adaptive plasticity andefficient evolutionaryresponse to selection

Figure 1. Extinctions and invasions conceptualized ‘Through the LookingGlass’ of evolutionary ecology. Extinctions (left side) represent populationdecline over time, while biological invasions (right side) represent an increasein abundance. Both invasions and extinctions reflect a common set ofelements (central column) because subtle but influential ecological and gen-etic differences (outer columns) can cause opposite population growthtrajectories. (Online version in colour.)

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beneficial when isolation is prolonged and population sizesare especially small; however, the benefits of increasing geneflow must be evaluated relative to the risk of compromisinglocally adapted genotypes.

Because the efficacy of selection is directly proportional toNe, genetic drift has a much stronger effect on evolutionarychange in species with limited genetic variability andamong small, isolated populations, compared with largerwell-connected populations. The reduced ability to respondto selection makes endangered populations particularlysusceptible to environmental changes that lead to loss oflocal adaptation. Here too, the metapopulation context dis-tinguishes biological invasions and provides additionalopportunities for these species to respond to selection despitefounder effects and genetic drift during establishment.Response to selection is more likely for invasive populationswhen (i) population sizes are large or increasing, (ii) geneflow from neighbouring populations acts as a genetic or evol-utionary rescue, and (iii) local extinction of maladaptedpopulations are followed by recolonization from populationswith pre-adapted genotypes. This latter example of inter-demic selection within a meta-population context occurs as aresult of non-random extinction and recolonization; this maybe an under-appreciated mechanism for rapid evolution ofinvaders in novel environments [23,25]. In this way, invasionsmight be useful experimental systems for understanding howpopulation connectivity contributes to the survival of individ-ual subpopulations in variable environments, applying thisknowledge in turn to restoration strategies and expectationsfor native species. Population genetic models that assignsource populations to colonists and test for genetic associ-ations between source population characteristics (e.g.density, inbreeding rate and phenotypes) and colonizationprobability may be a particularly useful approach for investi-gating the effect of metapopulation context on populationpersistence [24,26].

It is important to recognize that the genetic consequencesof small population size affect variation at neutral marker locidifferently than quantitative genetic variation in ecologicallyimportant traits, and indeed these two types of variance areoften poorly correlated [27]. This is likely a consequence ofthe broadly polygenic basis of most quantitative traits, asindividual loci each have only a small effect on the overalltrait variance. Previous studies have shown that substantialquantitative genetic variation (VG) can persist for quantitativetraits, even when populations show evidence of bottlenecksat individual loci [28,29]. As a result, rapid populationgrowth of invasive species following even a severe demo-graphic bottleneck will have little effect on quantitativegenetic variance [30]. Moreover, given that most introduc-tions fail, repeated founding events create opportunities fornatural selection to filter the genetic variants that do establishat the scale of genotypes or even entire populations [31],though direct evidence of this process is lacking to date. Bycontrast, persistent small population sizes over multiple gen-erations in endangered species will erode quantitative geneticvariance through genetic drift, limiting adaptive evolutionaryresponses to changing selection pressures. Few studies havedirectly addressed the consequences of invasion or coloniza-tion on VG, although one such study showed a loss of VG inyounger colonizing populations during (non-invasive) rangeexpansion [32]. A few studies have compared VG betweennative and introduced populations of invasive species

[33,34], but in these cases it is difficult to rule out differencesamong populations in the strength of stabilizing selection.Increasingly, population genomics is enabling the discoveryof genes (or closely linked loci) involved in local adaptation,which may allow a more direct integration of molecular datainto conservation strategies. More generally, genomic sequen-cing can now be combined with ecological surveys and fieldmanipulations to better understand the relationship betweengenome-wide genetic variation and adaptive trait variation innatural populations, and how both are affected by demo-graphic bottlenecks, gene flow and natural selection.

(b) Genetic load and inbreeding depressionOne intriguing difference between endangered and invasivespecies is the effect of small population size on genetic loadand inbreeding depression. Genetic load is a well-establishedconservation concern for many endangered taxa, as elevatedinbreeding in small populations exposes the negative fitnesseffects of recessive deleterious alleles [17]. These effectsdirectly contribute to increased extinction probability,especially under stressful environments [35]. The genome-wide load of deleterious mutations is sensitive to Ne, whichdetermines how effectively purifying selection can purgegenetic load. In endangered populations that are small,declining, or have undergone a bottleneck, avoiding or miti-gating inbreeding is critical to maintain genotypes that carryfew deleterious alleles (e.g. avoiding Muller’s Ratchet). Inva-ders may also suffer from inbreeding depression if acolonization bottleneck is severe, as exemplified by a multi-species analysis of birds introduced to New Zealand. In thiscase, species that experienced strong bottlenecks (less than150 individuals) showed persistent increases in hatching fail-ure compared with less ‘bottlenecked’ species [36]. Theseeffects may be transient in growing populations as someempirical studies have found increases in heterozygosityover time, despite bottlenecks as severe as a single pair ofbreeding individuals [37,38]. This is consistent with anincrease in the efficiency of natural selection to ‘weed out’homozygous individuals as population sizes increase. How-ever, further studies are needed to determine whether thisis a general phenomenon in successful invaders. Invasivespecies may also accumulate genetic load as a by-productof the range expansion process. Recent theoretical work hasshown that small populations at the wavefront of an expand-ing range face increased probabilities of deleteriousmutations drifting to high frequency, termed ‘expansionload’ [39]. The accumulation of expansion load is predictedto lead to legacies of reduced fitness following expansion[40,41]. Long-range dispersal between multiple introductionsfrom distinct genetic sources could partially mitigate thiseffect by helping to shelter the genetic load in recentlyexpanded invasive populations [42], but to our knowledgethis has not been explored in colonization models.

Why do invasive populations not suffer from inbreedingdepression more often? First, as described above, if invadersrecover from demographic bottlenecks more quickly, theymaintain genetic variation and experience less severe geneticdrift and inbreeding. Second, as invasive populations grow inNe, selection should become more effective at reducing thefrequency of weakly deleterious alleles, thereby reducingthe genetic load [43]. Third, the fitness effects of recessivealleles may be conditional on the environment. Phenotypic

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effects of deleterious mutations may be conditionally neutralwhen the environment is benign but amplified by environ-mental stress, resulting in inbreeding " environment (I " E)interactions [44]. Invasive species tend to experience morebenign environments than endangered species, for example,by invading resource-rich or enemy-free environments, andthis could mask the expression of deleterious alleles [45].Consequently, invasive species may avoid the negative fitnesseffects of inbreeding more often than rare and decliningspecies, even when subject to the same evolutionarydynamics of small population size. An important questionis thus how much of the among-population variance in fit-ness (and underlying allele frequency differentiation) iscaused by different degrees of purifying selection acting onweakly deleterious or conditionally neutral (I " E) geneticload? Answering this question could improve insights intothe population-level consequences of different amounts ofinbreeding in both invasive and endangered species. Spatialcomparisons of population demography could be coupledwith experimental and/or genomic assessments of geneticload to assess the conditions associated with effective pur-ging. Here, an experimental strength is the high replicationpotential afforded by many invading populations withdifferent demographic histories.

(c) The pros and cons of genetic admixtureAdmixture is a well-established outcome for invasions andarises when multiple genotypes from genetically divergentpopulations in the native range come into secondary contactduring invasion [46–48]. Hybridization and admixture arealso a major issue for species at risk, where decliningpopulations may be intentionally admixed during manage-ment efforts or may unintentionally hybridize with moreabundant species [49,50]. The immediate fitness consequencesof admixture can be complex, depending on the degreeof divergence of the parental lineages, and can vary amongF1 and more advanced recombinant hybrid generations[51,52]. Fitness effects can range from highly beneficial out-breeding to severely deleterious hybrid incompatibilities,decreasing in benefit as parental populations become morelocally adapted [53].

A distinct benefit of admixture for both invasive andendangered species is increased heterozygosity at loci con-taining recessive deleterious mutations. Positive effects ofadmixture have been observed in invasive populationsthat show heterozygosity-fitness correlations in the intro-duced range [46,54]. The fitness benefits of a heterozygousgenome are likely to be especially strong for small, decliningand inbred populations of endangered species that are unableto purge deleterious mutations [55]. This is frequently seen inzoo or other extremely bottlenecked vertebrate populations.For example, the endangered Florida panther populationshrank in size to as few as 20 individuals, with reduced het-erozygosity at neutral markers and phenotypic evidence ofinbreeding depression, including sperm deformities, kinkedtails and reduced survival [56]. Intentional release of eightfemale Texas pumas into Florida created opportunities foradmixture, doubling heterozygosity in the population andalleviating inbreeding depression in many traits.

In many cases, admixture also contributes to increases instanding VG and can broaden the genotypic space availableto selection. When adaptive variants from a genetically

distinct population introgress, natural selection can act onthis enhanced standing variation without waiting for newmutations to arise de novo [57]. For these reasons, and becauseinvasive species frequently experience novel selectiveenvironments in their introduced range, admixture hasbeen implicated as a potential factor fuelling rapid evolutionand the generation of novel invasive genotypes [33,48,58].Nevertheless, direct evidence of a link between introgressedvariation and the evolution of invasiveness is largely lackingto date. Population genomic studies of admixture/hybridzones during invasions could test the adaptive introgressionhypothesis using methods that identify the signal of differen-tial introgression of positively selected loci against the nullexpectation based on the degree of admixture across thegenomic background (e.g. genomic clines analysis) [59]. Thebenefit of adaptive introgression should be most pronouncedwhen rates of gene flow and introgression are low relative toNe and recombination rate, such that selection can efficientlyincorporate beneficial variants while eliminating detrimentalalleles. Therefore, adaptive introgression of positivelyselected genomic regions is likely to be much less commonin endangered species, where low population sizes andlow effective recombination limit the ability of selection todecouple maladaptive from adaptive introgressed alleles.

Populations of endangered species can also benefit fromexpanded genotypic variation resulting from admixture.Indeed, this is one reason that wildlife corridors are promotedfor conservation [60]. The benefit of admixture is reducedwhen populations are locally adapted and therefore may beless beneficial for native relative to non-native species. Suchan influx of genetic variation would be even more detrimentalin small populations where natural selection is less efficient ateliminating locally maladapted alleles [61,62]. This genomicswamping of endangered species has become a serious con-servation concern when small native populations meetabundant populations of reproductively compatible invasivespecies. Many native species show relatively low reproductiveisolation from introduced species with which they have hadno historical contact, and high numbers of introduced geno-types increase the likelihood of hybridization [63,64]. Inaddition to swamping locally adapted alleles, these native-invasive hybrids can put legal protections of native speciesin jeopardy as species definitions become questionable [65].

3. Phenotypic plasticityThe developmental, physiological and life-history modifi-cations that have been widely observed in natural populationsexposed to altered or novel environments can be due to plasticresponses of individuals in a population as well as to selectivetrait changes [66,67]. To focus on this aspect of diversity, eachgenotype can be viewed as a repertoire of phenotypesexpressed in different environments, or, more technically, anorm of reaction. This perspective makes it possible to evaluateboth individual adaptive flexibility and genetic variation asexpressed in novel environments. It is important to distinguishadaptive plastic responses, which maintain fitness across arange of environments, from phenotypic responses that arisedirectly from resource limits or other stresses and may not beadaptive. Reaction norms are products of evolution that, likeany phenotypic trait, are inevitably subject to developmental,phylogenetic and genetic constraints [68]. Consequently,

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individual plasticity is best understood as the result of adaptiveand stochastic evolution, rather than as a separate phenomenon[69]. Individual plasticity can play two key roles in the eco-evolutionary dynamics of natural populations. First, thecapacity of individuals to express adaptive plasticity inresponse to novel or changing environments contributes to apopulation’s viability. Second, existing norms of reaction, andgenetic variation for these norms, influence the potential forfuture evolution of adaptive responses to new environments.

(a) Plasticity and tolerance of novel environmentsAdaptive plasticity allows individual organisms to surviveand reproduce in a variety of environmental conditions.Such plasticity can buffer populations or species from extinc-tion when conditions change rapidly [70–72]. For example,some birds and mammals can advance life-history schedulesthrough plastic responses to seasonal cues, allowing them tokeep pace with altered timing of food availability due torapid climate change (e.g. [73]); the many taxa whose popu-lations lack such plasticity may face an enhanced risk ofextinction [74,75]. Adaptive plasticity can include effects ofparental environments on offspring phenotypes (transgenera-tional plasticity). For instance, in the sheepshead minnow,offspring growth rates, body mass and expected fecunditywere highest at temperatures previously experienced byparent fish, regardless of whether that temperature washigh or low [76]. As a result, warmer water temperaturesdid not cause negative effects on development and fitness.Adaptive transgenerational effects such as this may be mostbeneficial to species encountering gradual changes in theenvironment, including the rise in sea temperatures predictedunder current models of global climate change.

Along with promoting species persistence, adaptive plas-ticity can facilitate the rapid spread of invasive species acrossdiverse new habitats [77–79]. In both animals and plants, theability to maintain net reproductive rates in contrastingenvironments promotes invasive spread [80,81]. Addition-ally, a plastic response to sharply increase fecundity inresource-rich environments may be an important attributeof invasive taxa [82,83] because it increases the ‘propagulepressure’ that fuels colonization [84,85]. Theoretical workindicates that greater adaptive plasticity should be associatedwith higher rates of colonization of new, and more diverse,environments [86]. However, recent meta-analyses disagreeas to whether invasive species consistently show higherplasticity in general than native congeners [82,87]. This incon-sistency in part reflects the different plasticity metrics andchoice of traits used in various studies. Results of nativeversus invasive comparisons also depend on environmentalvariability in the home range that favours high plasticity,and on norm of reaction evolution following a species’introduction (for instance, canalization of a new adaptivephenotype following initially high plasticity) [88].

In addition to maintaining fitness across environments,adaptive plasticity can prevent a decrease in ecologicalbreadth when a genetic bottleneck occurs, as each genotypecan accommodate diverse conditions. Such plasticity canmitigate the ecological consequences of a prolonged bottle-neck in an endangered species [89] or a short-termbottleneck due to an introduction event [90,91]. In thesecases, geographically isolated populations may share similarbroad patterns of individual plasticity instead of divergent,

locally adapted norms of reaction [92,93]. However, as adap-tive plasticity itself has a genetic basis, it can be compromisedby the negative consequences of inbreeding and sustainedbottlenecks. Moreover, two critical factors will determinethe effectiveness of plasticity relative to selective evolutionin maintaining the viability of populations exposed to novelenvironments. First, norms of reaction that evolved underpast selection pressures may not encompass the range of phe-notypes required to maintain fitness in the new circumstances,and can even produce a disrupted, maladaptive phenotype inresponse to a novel stress [94]. Second, even with sufficientexisting plasticity, adaptive phenotypes will not be producedif changed cues fail to provide accurate information to elicitappropriate and timely responses [69,95]. In such cases,plasticity can promote extinction rather than persistence[29]. This potential adaptive limit may be particularly impor-tant in human-altered environments or following introductionto a new continent where abiotic and biotic factors thatorganisms have evolved to use as plasticity cues may beabsent or disrupted.

(b) Plasticity and evolutionary potentialPhenotypic plasticity can allow a population to persist fol-lowing a change in local conditions or introduction to anew range. If pre-existing reaction norms do not produce suf-ficiently adaptive phenotypes to maintain a population’sviability (e.g. [96]), then further adaptive evolution of plas-ticity is an essential step to either avoid extinction or permitestablishment (modelled by Chevin & Lande [97]; see[98–100] on selective evolution of reaction norms). In inva-sive species, rapid plasticity evolution can promotesubsequent spread into new habitats. For instance, canetoads (Rhinella marina) that have spread to colder regions inAustralia have evolved higher metabolic plasticity [101];invasive freshwater populations of the marine-native cope-pod Eurytemora affinis have evolved increased ion-transportplasticity [96]; and a shrubby South African Senecio intro-duced into Spain has evolved greater reproductive outputin wet conditions without any loss of fitness in its ancestraldry habitat [102].

Expanded repertoires of adaptive plasticity can result fromthe environmental heterogeneity encountered within andamong sites in the new range, rather than from a changeddirectional selection pressure compared to the native range[103]. This finding is consistent with theoretical predictionsthat increased adaptive plasticity is selectively favoured inpopulations and metapopulations that encounter variableenvironments ([68,86,104–108] and references therein). Thisparticular selective property may lead to a positive evolution-ary feedback for greater invasiveness in non-native taxa thathave sufficiently broad norms of reaction to survive theirinitial introduction. Because successful non-natives tend to(i) colonize disturbed, variable habitats and (ii) have high dis-persal capabilities that would cause them to encounter diversesites, they may be especially likely to evolve greater adaptiveplasticity post-introduction [109]. Evolution of increasinglygeneralist norms of reaction will in turn promote an evenbroader ecological distribution across habitats ([67] and refer-ences therein), expanding the invasion front and possiblycreating more contiguous populations that will accelerate colo-nization of new sites [85,110]. Conversely, if endangered taxainitially have less-plastic norms of reaction that confine them

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to a narrow range of conditions, they may not encounter theenvironmental variability that promotes evolution of broaderplasticity.

Although a cost of plasticity could in theory limit this typeof evolution, evidence for such a cost is weak [107,111], andrecent models assume that any plasticity costs are out-weighed by benefits (e.g. [97]). Indeed, the previousexamples show that increasingly broad adaptive norms ofreaction can evolve, at least in certain taxa, without fitnesstrade-offs that would entail a loss of adaptive responses toancestral environments. In any given case, the evolution ofgreater plasticity—like that of any adaptive trait—dependson whether or not genetic or developmental constraints arepresent that limit the potential for selective change. Howwidespread among invasive taxa is the potential to evolve‘jack of all trades’ genotypes? Is the lag phase between intro-duction and invasion commonly characterized by theevolution of greater adaptive plasticity? These questions canbe explored through resurrection experiments designed tocompare environmental response patterns of genotypessampled from introduced taxa across time (e.g. [103]).

As with any phenotypic trait, evolution of plasticityrequires genetic variation—in this case, genetic differences inreaction norms measured as genotype " environment (G " E)variance in a statistical model ([67,68,112,113] and referencestherein). Like other aspects of genetic diversity, populationsand taxa will differ in G " E variation due to previousmutation, drift and selection. A defining feature of G " Evariation is that a given set of genotypes may express differentphenotypes in certain environments, but converge on similarphenotypes in others: in other words, genetic variance itselfdiffers from one environment to another [114,115]. A novelenvironment such as a new range or altered habitat can leadto rapid adaptive evolution if genotypes in a populationexpress different phenotypes [116]. By contrast, evolutionaryresponse to natural selection is buffered in a new environmentwhere similar phenotypes occur [69,95,117]. Consequently,differences in patterns of G " E variation will influence theability of populations to evolve new adaptive responses fol-lowing introduction or in situ environmental challenges. Inaddition, a better understanding of the genetic architecturesunderlying reaction norms, such as the effects of modularityversus pleiotropy of regulatory pathways [118], will betterinform models of constraint on plasticity evolution in naturalpopulations [67,119].

In general, it is not known whether phenotypes in naturalpopulations are more likely to differ or converge in predictedfuture environments such as high CO2 and higher tempera-tures [120,121]. The question of adaptive evolutionarypotential is of particular concern with respect to speciesthat may face extinction in the absence of altered plasticitypatterns. A case in point is reptiles with temperature-dependent sex determination, which are predicted to producefemale-biased sex ratios in warmer future climates [122]. In astudy of the leopard gecko Eublepharis macularius [123], popu-lations were found to contain G " E variation for theproportion of males produced at different likely incubationtemperatures. Such variation could fuel the selective evol-ution of new temperature thresholds for sex determinationin future populations, promoting the species’ persistence.Similarly, certain European populations of great tits (Parusmajor) contain genetic variation for temperature-based plas-ticity of reproductive timing, providing the potential for

adaptive evolution of life-history plasticity in response toaltered seasonal timing of food availability [124]. Examiningnorm of reaction diversity in populations of various organ-isms, including its expression under predicted futureconditions, is a crucial step to assess (i) the potential forplasticity evolution to prevent extinction and (ii) the criticaldifferences in evolutionary potential between endangeredand invasive species.

4. Ecological nicheInvasive and endangered species exist at opposite ends ofecological spectra in geographical range size, niche breadthand population density [125–127] (figure 1). Geographicalrange size correlates positively with both local abundance[128,129] and niche breadth [130]. Therefore, understandingeco-evolutionary constraints on the ecological niche andlocal abundance could improve our understanding of whysome species remain rare while others become invasive[127]. We use the term ‘ecological niche’ in the broad sense,as the range of environmental conditions and resources thatinfluence the viability of local populations, either in theabsence (fundamental niche) or in the presence (realizedniche) of biotic interactions [131]. In this section, we applythe eco-evolutionary framework to the ecological niche con-cept and ask how differences in genetic variation andplasticity might explain niche differences in invasive andendangered species.

Some invasive species have evolved rapidly alongenvironmental gradients during range expansion, increasinggenetic variation for ecologically important traits and poten-tially expanding the niche well beyond that of the founderpopulation(s). For example, clinal genetic variation in traitssuch as size and phenology have been documented in anumber of widespread invasive species across geographicalgradients, including latitude (e.g. [132]), elevation (e.g.[133]) and continentality (e.g. [134]). Interestingly, a species’climatic niche breadth in its non-native range often doesnot exceed its niche breadth in the native range—in otherwords, climatic niches are frequently conserved betweenranges [135]. This raises a biological conundrum: if intro-duced populations evolve and plasticity allows persistencein a range of environments, why are similar climatic limitsre-established in introduced populations [136]?

One explanation is the presence of constraints on nichebreadth along environmental gradients that are also con-served across ranges [137]. Genetic constraints on nichebreadth could include inbreeding depression, maladaptivegene flow or low heritable genetic variability in singletraits, and also along multivariate trait axes (i.e. core trade-offs; reviewed by [138,139]). Core trade-offs provide perhapsthe most convincing explanation for why niche limits shouldbe conserved across disparate geographical ranges, despitethe evolution of local adaptation [136]. For example, naturalselection favours early flowering time and larger size at flow-ering across the native and introduced ranges of Lythrumsalicaria, but evolution of these traits is constrained by atrade-off [132,140]. This trade-off limits the reproductiveoutput of earlier flowering plants in high-latitude popu-lations, helping to set the northern range limit in both thenon-native and native ranges. Therefore, while adaptive evol-ution during invasion can contribute to the niche expansion

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of founder populations, genetic architecture can limit theextent of adaptive evolution and niche breath. As outlinedin previous sections, several genetic attributes of non-nativepopulations promote adaptive evolution of niche breadth.By contrast, high genetic drift, genetic load and small popu-lation will limit adaptive responses and could contribute tonarrow niche breadth in endangered species.

In addition to selection from abiotic factors, biotic inter-actions can influence range margins [141], and are likely todiffer in importance between native and introduced rangesas well as between invasive and endangered species. Thereare several mechanisms by which negative interactions (e.g.competition or predation) could contribute to evolutionaryconstraints on niche breadth (figure 2). First, if selectionimposed by species interactions is antagonistic to abioticselection pressures, this can limit the fitness of local popu-lations and ultimately restrict niche breadth. This wouldoccur if either the same trait was under antagonistic selectionfrom abiotic and biotic factors, or if multiple genetically cor-related traits were under antagonistic selection. For example,the evolution of increased competitive ability (EICA) hypoth-esis predicts a trade-off between herbivore defence andcompetitive ability in plants [142]. Non-native species thatescape regulation by natural enemies, particularly specialists,would therefore experience relaxed selection on traits associ-ated with defence, allowing a response to selection for

increased competitive ability. While there is support for theEICA hypothesis in some species [143], the consequencesfor niche breadth in the non-native range of invasive specieshave, to our knowledge, not been investigated. Second,resource competition can constrain niche evolution by impos-ing strong selection against resource switching (i.e. stabilizingselection) even as resource availability drops to unsustainablelevels [144,145]. Third, competition that reduces fitness of afocal species can suppress the expression of genetic variationfor ecologically important traits, limiting the potential forselective changes in niche breadth. In an elegant experimentacross a depth gradient in Californian vernal pools, releasefrom competition enabled the annual plant Lasthenia fremontiito expand its niche breadth, and exposed additive geneticvariation in the fundamental niche for which there was posi-tive selection [146]. These examples suggest that a relaxationin evolutionary constraints caused by biotic interactions islikely to facilitate niche expansion, and could contribute tothe success of invasive species that experience ecologicalrelease from native-range competitors or natural enemies.By contrast, biotic interactions might impose particularlystrong evolutionary constraints on endangered species withnarrow niche breath, compounded by low genetic variationor plasticity in traits affecting the outcome of interactions.

Ecological release is a common explanation for why someinvasive species attain higher abundance in their new range

native range

stabilizing selection trait variance suppressionantagonistic selection

trait value

niche axis 1

niche

axis

2

fitn

ess

freq

uenc

y

fitn

ess

fitn

ess

trait value

with biotic interaction without biotic interaction

trait value

(a)

(b)

non-native range

Figure 2. Eco-evolutionary model of the ecological niche as an emergent property of genetic constraints and spatial variation in abiotic and biotic sources of naturalselection. (a) The number of individuals in a population ( y-axis) depends on environmental variables that vary along geographical gradients (niche axes 1 and 2), forexample, moisture and temperature. Additional constraints on the niche of the focal species (darker green plant) are imposed by negative biotic interactions, such asa competitor (lighter yellow plants). Escape from negative biotic interaction represents an ecological release, which increases population vital rates across a range ofenvironments and thereby expands the ecological niche. (b) Three evolutionary consequences of relaxed biotic interactions for an individual population, measurednear the edge of the range of the focal plants (black circles in (a)). Selection at this location is measured either in the presence (lighter blue curve) or in the absence(darker red curve) of competition: antagonistic selection—ecological release relaxes antagonistic selection on a trait that is also under abiotic selection (e.g. phenol-ogy) or on a genetically correlated trait (e.g. size at reproduction); stabilizing selection—ecological release relaxes the strength of stabilizing selection across a rangeof trait values; trait variance suppression—competition suppresses the expression of heritable genetic variation, which increases following ecological release. In thefirst two cases, ecological release is also accompanied by an increase in absolute fitness as negative selection pressures are removed.

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[147], and release from negative interactions with competitorsand pathogens even appears to have allowed some non-native species to expand their realized niches [148–150].Indeed, there are examples of species that are consideredendangered in their native range, sometimes restricted to afew populations, yet can attain broad non-native ranges (e.g.plants used in horticulture or forestry such as Pinus radiata,Lotus maculatus, Melaleuca quinquenervia) [149,151,152]. Nicheexpansion following invasion is usually interpreted as apurely ecological response to an altered biotic environment;the possible contribution and relative importance of evolutionand phenotypic plasticity, though acknowledged, is rarelytested [149]. Hill et al. [153] showed that niche shifts are associ-ated with the evolution of thermal tolerance in the mite,Halotydeus destructor, in Australia. Evolution has also beenassociated with the invasion of a narrowly endemic CanaryIsland shrub across large parts of California [34]. Anotherform of niche expansion is host shifting in herbivorous insects,including those introduced for biocontrol. For example, non-native populations of the beetle Ophraella communa in Japanhave evolved to use Ambrosia trifida as a host, even thoughthis plant is not used by O. communa in its native range.This host shift is partly explained by relaxed herbivoredefences in non-native populations of A. trifida, after havingescaped natural enemies for approximately 50 generations[154]. However, the contribution of relaxed selectionto niche expansion and the role of genetic constraints arestill unresolved.

Overall, endangered species can be predicted to experiencestronger constraints on niche breadth than invasive taxa forseveral reasons. First, endangered species might experiencegreater genetic constraints than invasive species for reasonsoutlined in the previous sections (e.g. genetic bottlenecksand inbreeding). Second, endangered species might be charac-terized by especially strong negative biotic interactions.Indeed, invasive and endangered species can be discriminatedby the strength of negative interactions with pathogens [155]and competitors [156]. Nonetheless, while rapid evolutionassociated with environmental gradients is recognized asbeing important for the persistence of endangered species inchanging environments [157] and for the dynamics of speciesinvasions [158], we know much less about the contribution ofchanging biotic interactions to niche evolution in invasive andendangered species [159]. Understanding whether negativebiotic interactions impose constraints on niche evolution, inaddition to a purely ecological restriction of niche breadth, isimportant for accurately predicting evolutionary responses ofendangered and invasive species experiencing novel andchanging environments.

5. Conclusion and future directionsLike Lewis Carroll’s looking glass, endangered and invasivespecies appear similar at first glance, as both often (i) experi-ence strong demographic bottlenecks, (ii) are subject tohybridization and introgression from other species or diver-gent populations, and (iii) encounter fitness challenges dueto novel and changing environments. Yet these apparentlysimilar reflections differ in key elements that lead to verydifferent eco-evolutionary realities. Specifically, the potentialfor adaptive evolution of phenotypes and broad individualplasticity is predicted to be higher in invading species as a

result of (i) rapid population growth following transientdemographic bottlenecks, (ii) lower genetic load, (iii) greaterenvironmental variability, and (iv) relaxed selection fromnatural enemies and competition. These evolutionarydifferences directly affect the breadth of the realized ecologi-cal niche and ultimately determine the abundance anddistribution of species in nature.

Our discussion identifies key elements of what we believecould be a robust framework for exploring eco-evolutionarydynamics using comparative studies of invasive and endan-gered species. Contrasting invasive and rare or endangeredspecies is not a novel concept, but has tended to focus oninterspecific comparisons of functional traits rather than onthe local ecological and demographic conditions that directlyinfluence population dynamics. Understanding limits toadaptive evolution (including appropriate plasticity patterns)at the population level may be a more promising avenue ofresearch. We believe these kinds of comparisons betweenendangered and invasive species represent an under-exploitedopportunity to better understand and manage the abundanceand distribution of species at both ends of the ecologicalspectrum. Experimental manipulations could compare pheno-typic selection, reaction norms, neutral and functional geneticdiversity of closely related endangered and invasive species inseveral different environments to better understand evolution-ary potential and constraints. Endangered (or at least rarenative) species that are invasive or spreading elsewherewould be particularly useful study systems to investigate inthis way.

One potential obstacle to developing such a framework isthe fact that researchers investigating invasive and endan-gered species rarely collaborate—indeed the authors of thispaper work primarily on invasive species and as a resultour discussion is more heavily weighted towards this area.Nevertheless, we hope that this review will encouragebetter communication between these two fields. After all,the goals of conserving endangered species and preventinginvasions both require a comprehensive understanding ofthe evolutionary and ecological factors that affect populationpersistence in a changing world. Combining knowledgegained from the thousands of published ecological, evolution-ary and population genetic studies of invasive and endangeredspecies could lead to more robust tests of theoretical foun-dations of conservation biology, and to a comprehensive,unified framework for the management of global biodiversity.

Authors’ contributions. All authors contributed to the conceptual devel-opment, writing and revising of the manuscript. R.I.C. initiatedand coordinated the project, and all other authors contributedequally.Competing interests. We have no competing interests.Funding. R.I.C. is funded by Canada Research Chair (CRC) and aDiscovery Grant from the Natural Sciences and Engineering ResearchCouncil of Canada (NSERC). K.M.D. is funded by a United StatesDepartment of Agriculture (USDA) grant no. 2015-67013-23000.S.R.K. is funded by a USDA Cooperative Agreement project no.8062-22620-004-17S. S.E.S. is funded by the New Phytologist Trust.J.M.A. is supported by ETH Zurich funding to the Plant Ecologygroup.Acknowledgements. The authors are grateful to A. Hendry, K.Gotanada andE. Svensson for the invitation to contribute to this special issue and sug-gestions that improved the manuscript. We are also grateful forconceptual discussions and manuscript suggestions fromS. Yakimowski.

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